Benefit of pulsation in soft corals Maya Kremiena,b,1, Uri Shavitc, Tali Massa,d,e, and Amatzia Genina,e aHeinz Steinitz Marine Biology Laboratory, Interuniversity Institute for Marine Sciences, Eilat 88103, Israel; bInstitute of Earth Sciences and eDepartment of Ecology, Evolution, and Behavior, Alexander Silberman Institute of Life Sciences, Hebrew University of Jerusalem, Jerusalem 91904, Israel; cCivil and Environmental Engineering, Technion, Haifa 32000, Israel; and dInstitute of Marine and Coastal Sciences, Rutgers, State University of New Jersey, New Brunswick, NJ 08901 Edited by Tom M. Fenchel, University of Copenhagen, Helsingor, Denmark, and approved March 27, 2013 (received for review February 1, 2013) Soft corals of the family Xeniidae exhibit a unique, rhythmic ribulose-1,5-bisphosphate carboxylase oxygenase (RuBisCO) (10), pulsation of their tentacles (Movie S1), first noted by Lamarck thereby increasing the rate of photosynthesis by the coral’s endo- nearly 200 y ago. However, the adaptive benefit of this perpetual, symbiontic algae (9). Our study of the above predictions, including energetically costly motion is poorly understood. Using in situ un- a characterization of the pulsation rhythm and its hydrodynamic derwater particle image velocimetry, we found that the pulsation effects, was carried out with the xeniid coral Heteroxenia fuscescens motions thrust water upward and enhance mixing across the (Fig. 1) from the coral reef of Eilat, Red Sea, where this and several coral–water boundary layer. The induced upward motion effec- other xeniid species are common (10, 11). tively prevents refiltration of water by neighboring polyps, while the intensification of mixing, together with the upward flow, Results greatly enhances the coral’s photosynthesis. A series of controlled Pulsation Cycles. Pulsation activity during day and night was ex- laboratory experiments with the common xeniid coral Heteroxenia amined in situ with four different H. fuscescens colonies at 5- to fuscescens showed that the net photosynthesis rate during pulsa- 10-m depth, using an underwater infrared (IR)-sensitive video tion was up to an order of magnitude higher than during the camera cabled to shore. Underwater IR illumination was used coral’s resting, nonpulsating state. This enhancement diminished during the night (Materials and Methods). The period of one full when the concentration of oxygen in the ambient water was arti- pulsation cycle was on average (±SD) 1.6 s (±0.18 s) (n = 72), ficially raised, indicating that the enhancement of photosynthesis with no phase synchronization among neighboring polyps within fl was due to a greater ef ux of oxygen from the coral tissues. By the colony (Fig. 1A). lowering the internal oxygen concentration, pulsation alleviates Complete diel (24-h) records obtained for three of the colo- fi the problem of reduced af nity of ribulose-1,5-bisphosphate car- nies showed that the corals pulsate continuously during most boxylase oxygenase (RuBisCO) to CO2 under conditions of high (>95%) of the time. Short (15–30 min) intervals without pulsa- – oxygen concentrations. The photosynthesis respiration ratio of tion (hereafter “rest”; Fig. 1B) were observed once a day, usually H. fuscescens the pulsating was markedly higher than the ratios in late afternoon (Fig. 2). The entire record (>350 h) showed reported for nonpulsating soft and stony corals. Although pulsa- fi that resting intervals always occurred when the intensity of solar tion is commonly used for locomotion and ltration in marine radiation was <50% of the daily maximum. mobile animals, its occurrence in sessile (bottom-attached) species is limited to members of the ancient phylum Cnidaria, where it is Pulsation, Respiration, and Photosynthesis. A comparison of res- used to accelerate water and enhance physiological processes. piration and photosynthesis between pulsating and resting H. fuscescens was carried out in the laboratory with freshly col- fi mass balance | diffusion | mass transfer coef cient | Red Sea lected colonies (Materials and Methods). As shown in Fig. 3, these measurements indicate that the coral’s respiration rate during unique characteristic of soft corals belonging to the family pulsation was approximately two times higher than during rest AXeniidae (phylum Cnidaria) is the perpetual, nonsynchro- periods (mean ± SD =×2.06 ± 0.28), whereas the gross photo- nous pulsation of the colony’s polyps (Movie S1). This unique synthesis was sevenfold higher (×7.11 ± 0.96); Fisher’s combined motion, consisting of a rhythmic extension and contraction of the probability test: P < 0.01, n = 3 measurements for each of the three tentacles, was first noted two centuries ago by Lamarck (1). colonies for each of the respiration and photosynthesis measure- However, neither its biomechanical effects nor its benefits to the ments. A similar pattern was found in a different experiment where coral are understood. To the best of our knowledge, no other we measured the change in net photosynthesis as function of sessile organism in the world’s oceans exhibits such a behavior. irradiance intensity (P–I curves). The results (Fig. 4) show that in The closest motion resembling this pulsation is exhibited by me- the pulsating corals the slope of the P–I curve was much steeper, dusae that rhythmically contract their bell (exumbrella) to swim reaching about an order of magnitude higher Pmax than in the (2, 3) or enhance nutrient uptake (4–6). resting corals. Here, the enhancement of photosynthesis was al- As pulsation in xeniid corals is vigorous and perpetual, its ready noticeable at dim light (3,500 lx), equivalent to the intensity benefit should be considerable. Because all xeniid corals host of light at 10-m depth about 1 h after sunrise or before sunset. symbiotic algae, and because food particles are rarely found in During pulsation, the stems of the active polyps are always their gastrovascular cavity (7, 8), a positive effect of pulsation on extended and their tentacles rhythmically change their posture carbon acquisition via photosynthesis of their symbionts or on from being fully extended in the open state, to being tightly the uptake of dissolved matter from the surrounding waters can be especially beneficial for these animals. Here, we measured the metabolic cost of pulsation and tested Author contributions: M.K., U.S., and A.G. designed research; M.K., U.S., T.M., and A.G. the hypothesis that the key benefits of pulsation are the en- performed research; U.S. and T.M. contributed new reagents/analytic tools; M.K., U.S., hancement of photosynthesis by the coral’s symbiotic algae and and A.G. analyzed data; and M.K., U.S., and A.G. wrote the paper. the prevention of water refiltration by neighboring polyps. The The authors declare no conflict of interest. proposed effect on photosynthesis is based on the prediction that This article is a PNAS Direct Submission. pulsation intensifies mixing and accelerates the flow over the coral– See Commentary on page 8767. water interface, which, in turn, increases the efflux of oxygen away 1To whom correspondence should be addressed. E-mail: [email protected]. ’ from the coral s tissues (9). The maintenance of low concentration This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. of oxygen inside the coral is expected to enhance CO2 binding by 1073/pnas.1301826110/-/DCSupplemental. 8978–8983 | PNAS | May 28, 2013 | vol. 110 | no. 22 www.pnas.org/cgi/doi/10.1073/pnas.1301826110 Downloaded by guest on September 25, 2021 Indeed, the increase in ambient oxygen practically eliminated the effect of pulsation on photosynthesis (Fig. 3B;Mann–Whitney, SEE COMMENTARY P = 0.51, n = 3 colonies, testing for a difference in gross photo- synthesis between pulsation under high oxygen and rest under normal oxygen). Note that the photosynthesis rate in the non- pulsating state was unaffected by the change in ambient oxygen (Mann–Whitney, P = 0.83, n = 3). Hydrodynamic Effects of Pulsation. The flow field generated by pulsation was recorded in situ using our custom-built un- derwater particle image velocimetry (UPIV) system (Materials and Methods), positioned at the reef so that the measurement domain was located above the center of the coral colony (Fig. S1). Pulsation markedly changed the flow pattern above the coral polyps (Fig. S1). Most noticeable was the vertical (up- ward) thrust driven by pulsation near the coral–water interface (Fig. S2A): whereas during rest the vertical velocity near that interface was weaker than that measured at 1.8 cm above the coral, under pulsating state the former velocity was about twice the latter. Lagrangian simulations were used to generate particle trajec- tories to further explore the flow patterns generated by pulsation. To do so, imaginary particles were “released” at the coral–water interface and tracked using our UPIV time series until they exited the measurement domain (Materials and Methods). As each trajectory started at the coral surface, where waterborne commodities such as dissolved gasses and nutrients are taken up by the coral, the simulation allowed us to assess the effect of pulsation on the probability of water refiltration by neighboring polyps. The results show that pulsation substantially reduced that probability; whereas in resting corals >50% of the imagi- nary particles (of a total of 1,379 trajectories) were refiltered at least once (Fig. 5 B and D), less than 20% of the trajectories (of fi A a total of 4,949) showed re ltration during pulsation (Fig. 5 ECOLOGY and C). Moreover, during pulsation the frequency distribution Fig. 1. The Xeniid coral Heteroxenia fuscescens during pulsation (A) and rest (B). Note the different postures of the tentacles among the pulsating polyps, demonstrating the absence of phase synchronization among the polyps within the colony. (C) A schematic illustration of the stem and ten- tacles of a single polyp. packed in the closed posture (Fig. 1 and Movie S1).